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GATA2 mitotic bookmarking is required for definitive haematopoiesis

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  • Rita Silvério-Alves

    (Lund University, BMC A12
    Lund University, BMC A12
    University of Coimbra, Largo Marquês do Pombal
    University of Coimbra, Largo Marquês do Pombal)

  • Ilia Kurochkin

    (Lund University, BMC A12
    Lund University, BMC A12)

  • Anna Rydström

    (Lund University, BMC A12)

  • Camila Vazquez Echegaray

    (Lund University, BMC A12
    Lund University, BMC A12)

  • Jakob Haider

    (Lund University, BMC A12
    Lund University, BMC A12)

  • Matthew Nicholls

    (University of Oxford)

  • Christina Rode

    (University of Oxford)

  • Louise Thelaus

    (Lund University, BMC A12
    Lund University, BMC A12)

  • Aida Yifter Lindgren

    (Lund University, BMC A12
    Lund University, BMC A12)

  • Alexandra Gabriela Ferreira

    (Lund University, BMC A12
    Lund University, BMC A12
    University of Coimbra, Largo Marquês do Pombal
    University of Coimbra, Largo Marquês do Pombal)

  • Rafael Brandão

    (University of Copenhagen, Blegdamsvej 3B)

  • Jonas Larsson

    (Lund University, BMC A12
    Lund University, BMC A12)

  • Marella F. T. R. Bruijn

    (University of Oxford)

  • Javier Martin-Gonzalez

    (University of Copenhagen, Blegdamsvej 3B)

  • Carlos-Filipe Pereira

    (Lund University, BMC A12
    Lund University, BMC A12
    University of Coimbra, Largo Marquês do Pombal)

Abstract

In mitosis, most transcription factors detach from chromatin, but some are retained and bookmark genomic sites. Mitotic bookmarking has been implicated in lineage inheritance, pluripotency and reprogramming. However, the biological significance of this mechanism in vivo remains unclear. Here, we address mitotic retention of the hemogenic factors GATA2, GFI1B and FOS during haematopoietic specification. We show that GATA2 remains bound to chromatin throughout mitosis, in contrast to GFI1B and FOS, via C-terminal zinc finger-mediated DNA binding. GATA2 bookmarks a subset of its interphase targets that are co-enriched for RUNX1 and other regulators of definitive haematopoiesis. Remarkably, homozygous mice harbouring the cyclin B1 mitosis degradation domain upstream Gata2 partially phenocopy knockout mice. Degradation of GATA2 at mitotic exit abolishes definitive haematopoiesis at aorta-gonad-mesonephros, placenta and foetal liver, but does not impair yolk sac haematopoiesis. Our findings implicate GATA2-mediated mitotic bookmarking as critical for definitive haematopoiesis and highlight a dependency on bookmarkers for lineage commitment.

Suggested Citation

  • Rita Silvério-Alves & Ilia Kurochkin & Anna Rydström & Camila Vazquez Echegaray & Jakob Haider & Matthew Nicholls & Christina Rode & Louise Thelaus & Aida Yifter Lindgren & Alexandra Gabriela Ferreira, 2023. "GATA2 mitotic bookmarking is required for definitive haematopoiesis," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40391-x
    DOI: 10.1038/s41467-023-40391-x
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    References listed on IDEAS

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    1. Mahé Raccaud & Elias T. Friman & Andrea B. Alber & Harsha Agarwal & Cédric Deluz & Timo Kuhn & J. Christof M. Gebhardt & David M. Suter, 2019. "Mitotic chromosome binding predicts transcription factor properties in interphase," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    2. Jean-Charles Boisset & Wiggert van Cappellen & Charlotte Andrieu-Soler & Niels Galjart & Elaine Dzierzak & Catherine Robin, 2010. "In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium," Nature, Nature, vol. 464(7285), pages 116-120, March.
    3. Dounia Djeghloul & Bhavik Patel & Holger Kramer & Andrew Dimond & Chad Whilding & Karen Brown & Anne-Céline Kohler & Amelie Feytout & Nicolas Veland & James Elliott & Tanmay A. M. Bharat & Abul K. Tar, 2020. "Identifying proteins bound to native mitotic ESC chromosomes reveals chromatin repressors are important for compaction," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    4. Vincenzo Calvanese & Sandra Capellera-Garcia & Feiyang Ma & Iman Fares & Simone Liebscher & Elizabeth S. Ng & Sophia Ekstrand & Júlia Aguadé-Gorgorió & Anastasia Vavilina & Diane Lefaudeux & Brian Nad, 2022. "Mapping human haematopoietic stem cells from haemogenic endothelium to birth," Nature, Nature, vol. 604(7906), pages 534-540, April.
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